Journal of Comparative Physiology A

, Volume 169, Issue 2, pp 165–176 | Cite as

Anatomy, neurophysiology and functional aspects of the nucleus isthmi in salamanders of the family Plethodontidae

  • Wolfgang Wiggers
  • Gerhard Roth
Article
Accepted:

Summary

Tongue-projecting plethodontid salamanders have massive direct ipsilateral retinal afferents to the tectum opticum as well as a large and well developed nucleus isthmi. Retrograde staining revealed two subnuclei: A ventral one projecting to the contralateral tectal hemisphere and a dorsal one projecting back to the ipsilateral side. The isthmic nuclei show a retinotopic organization, which is in register with that of the tectum. Electrophysiological recordings from nucleus-isthmi neurons revealed response properties that are very similar to those found in tectal neurons. Thus, there is no substantial processing of tectal neural activity in the nucleus isthmi. Measurements of peak latencies after electrical and light stimulation suggest the continuous coexistence of 4 representations of the visual field in the tectum mediated by (1) the contralateral and (2) the ipsilateral direct retinal afferents, (3) the uncrossed and (4) the crossed isthmo-tectal projection. (1) and (2) originate at the same moment in the retina and arrive simultaneously in the tectum. It is assumed that in plethodontid salamanders with massive ipsilateral retino-tectal projections depth perception based on disparity cues is achieved by comparison of these images.

Representations mediated by (3) and (4) arriving in the tectum at the same time as (1) and (2) originate 10–30 ms earlier in the retina. It is hypothesized that these time differences between (1)/(2) and (3)/(4) are used to calculate three-dimensional trajectories of fast-moving prey objects.

Key words

Nucleus isthmi Optic tectum Receptive fields Latencies Tectal maps Depth perception 

Abbreviations

EL

edge length

FDA

fluoresceine dextranamine

RDA

tetramethylrhodamine dextranamine

RF

receptive field

This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adams JC (1981) Heavy metal intensification of DAB-based HRP-reaction product. J Histochem Cytochem 29:775Google Scholar
  2. Antal M, Matsumoto N, Székely G (1986) Tectal neurons of the frog: Intracellular recording and labeling with cobalt electrodes. J Comp Neurol 246:238–253Google Scholar
  3. Caine HS, Gruberg ER (1985) Ablation of nucleus isthmi leads to loss of specific visually elicited behaviors in the frog Rana pipiens. Neurosci Lett 54:307–312Google Scholar
  4. Chung SH, Bliss TVP, Keating MJ (1974) The synaptic organization of optic afferents in the amphibian tectum. Proc R Soc Lond B 187:421–447Google Scholar
  5. Collett TS (1977) Stereopsis in toads. Nature 267:349–351Google Scholar
  6. Collett TS, Udin SB, Finch DJ (1987) A possible mechanism for binocular depth judgements in anurans. Exp Brain Res 66:35–40Google Scholar
  7. Dann JF, Beazley LD (1982) The development of connections between the isthmic nucleus and the tectum in Xenopus and Limnodynastes tadpoles. Neurosci Lett 33:107–113Google Scholar
  8. Fisher MD, Udin SB (1988) Connections between the nucleus isthmi and the tectum in larval and post-metamorphic axolotls. J Neurobiol 19:111–125Google Scholar
  9. Fite KV, Scalia F (1976) Central visual pathways in the frog. In: Fite KV (ed) The amphibian visual system. A multidisciplinary approach. Academic Press, London New York, pp 87–118Google Scholar
  10. Fritzsch B (1980) Retinal projections in European Salamandridae. Cell Tissue Res 213:325–341Google Scholar
  11. Gaillard F (1985) Binocularly driven neurons in the rostral part of the frog optic tectum. J Comp Physiol A 157:47–55Google Scholar
  12. Gimlich RL, Braun J (1985) Improved fluorescent compounds for tracing cell lineage. Dev Biol 109:509–514Google Scholar
  13. Glasser S, Ingle D (1978) The nucleus isthmus as a relay station in the ipsilateral visual projection to the frog's optic tectum. Brain Res 159:214–218Google Scholar
  14. Graybiel AM (1978) A satellite system of the superior colliculus: The parabigeminal nucleus and its projections to the superficial collicular layers. Brain Res 145:365–374Google Scholar
  15. Grobstein P, Comer C (1983) The nucleus isthmi as an intertectal relay for the ipsilateral oculotectal projection in the frog, Rana pipiens. J Comp Neurol 217:54–74Google Scholar
  16. Grobstein P, Comer C, Hollyday M, Archer SM (1978) A crossed isthmo-tectal projection in Rana pipiens and its involvement in the ipsilateral visuotectal projection. Brain Res 156:117–123Google Scholar
  17. Gruberg ER, Harris WA (1981) The serotonergic somatosensory projection to the tectum of normal and eyeless salamanders. J Morphol 170:55–69Google Scholar
  18. Gruberg ER, Lettvin J (1980) Anatomy and physiology of a binocular system in the frog Rana pipiens. Brain Res 192:313–325Google Scholar
  19. Gruberg ER, Udin SB (1978) Topographic projections between the nucleus isthmi and the tectum of the frog Rana pipiens. J Comp Neurol 179:487–500Google Scholar
  20. Grüsser OJ, Grüsser-Cornehls U (1976) Neurophysiology of the anuran visual system. In: Llinas R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 297–385Google Scholar
  21. Herrick CJ (1948) The brain of the tiger salamander Ambystoma tigrinum. The University of Chicago Press, ChicagoGoogle Scholar
  22. Jordan M, Luthardt G, Meyer-Naujoks C, Roth G (1980) The role of eye accommodation in the depth perception of common toads. Z Naturforsch 35c:851–852Google Scholar
  23. Keating MJ, Gaze RM (1970) The ipsilateral retinotectal pathway in the frog. J Exp Physiol 55:284–292Google Scholar
  24. Künzle H, Schnyder H (1984) The isthmus-tegmentum complex in the turtle and rat: A comparative analysis of its interconnections with the optic tectum. Exp Brain Res 56:509–522Google Scholar
  25. Larsell O (1967) The comparative anatomy and histology of the cerebellum from myxinoids through birds. University of Minnesota Press, MinneapolisGoogle Scholar
  26. Linden R, Perry VH (1983) Retrograde and anterograde transneuronal degeneration in the parabigeminal nucleus following tectal lesions in developing rats. J Comp Neurol 218:270–281Google Scholar
  27. Linke R, Roth G (1988) Neuroglial cells and axons in the optic nerve of lungless salamanders (Fam. Plethodontidae) In: Elsner N, Barth FG (eds) Sense organs. Thieme, Stuttgart, p 255Google Scholar
  28. Linke R, Roth G (1990) Optic nerves in plethodontid salamanders (Amphibia, Urodela): neuroglia, fiber spectrum and myelination. Anat Embryol 181:37–48Google Scholar
  29. Lombard RE, Wake DB (1976) Tongue evolution in the lungless salamanders, family Plethodontidae I. Introduction, theory and a general model of dynamics. J Morphol 148:265–286Google Scholar
  30. Lombard RE, Wake DB (1977) Tongue evolution in the lungless salamanders, family Plethodontidae II. Function and evolutionary diversity. J Morphol 153:39–79Google Scholar
  31. Luthardt-Laimer G (1981) Distance estimation in binocular and monocular salamanders. Z Tierpsychol 63:233–240Google Scholar
  32. Manteuffel G, Fox B, Roth G (1989) Topographic relationships of ipsi- and contralateral visual inputs to the rostral tectum opticum in the salamander Plethodon jordani indicate the presence of a horopter. Neurosci Lett 107:105–109Google Scholar
  33. Martinez S, Puelles L (1988) Avian nucleus isthmi ventralis projects to the contralateral optic tectum. Brain Res 481:181–184Google Scholar
  34. Naujoks-Manteuffel C, Manteuffel G (1988) Origins of descending projections to the medulla oblongata and rostral medulla spinalis in the urodele Salamandra salamandra (Amphibia). J Comp Neurol 273:187–206Google Scholar
  35. Northcutt RG (1982) Localization of neurons afferent to the optic tectum in longnose gars. J Comp Neurol 204:325–335Google Scholar
  36. Opdam P, Nieuwenhuys R (1976) Topological analysis of the brain stem of the axolotl Ambystoma mexicanum. J Comp Neurol 165:285–306Google Scholar
  37. Rettig G (1984) Neuroanatomische Untersuchungen der visuellen Projektionen bei Salamandern (Ordnung Caudata). Diss Univ BremenGoogle Scholar
  38. Rettig G (1988) Connections of the tectum opticum in two urodeles, Salamandra salamandra and Bolitoglossa subpalmata, with special reference to the nucleus isthmi. J Hirnforsch 29:5–16Google Scholar
  39. Rettig G, Roth G (1982) Afferent visual projections in three species of lungless salamanders (Family Plethodontidae). Neurosci Lett 31:221–224Google Scholar
  40. Rettig G, Roth G (1986) Retinofugal projections in salamanders of the family Plethodontidae. Cell Tissue Res 243:285–296Google Scholar
  41. Roldan M, Reinoso-Suárez F, Tortelly A (1983) Parabigeminal projections to the superior colliculus in the cat. Brain Res 280:1–13Google Scholar
  42. Roth G (1976) Experimental analysis of the prey catching behavior of Hydromantes italicus Dunn (Amphibia, Plethodontidae). J Comp Physiol 109:47–58Google Scholar
  43. Roth G (1982) Beuteerkennungsmechanismen im Tectum opticum von Amphibien — eine vergleichende Untersuchung. Funkt Biol Med 1:90–98Google Scholar
  44. Roth G (1982) Responses in the optic tectum of the salamander Hydromantes italicus to moving prey stimuli. Exp Brain Res 45:386–392Google Scholar
  45. Roth G (1987) Visual behavior in salamanders. Springer, BerlinGoogle Scholar
  46. Roth G, Naujoks-Manteuffel C, Grunwald W (1990) Cytoarchitecture of the tectum mesencephali in salamanders: A Golgi and HRP study. J Comp Neurol 291:27–42CrossRefGoogle Scholar
  47. Sakamoto N, Ito H, Ueda S (1981) Topographic projections between the nucleus isthmi and the optic tectum in a teleost, Navodon modes tus. Brain Res 224:225–234Google Scholar
  48. Sereno MI, Ulinski PS (1987) Caudal topographic nucleus isthmi and the rostral nontopographic nucleus isthmi in the turtle, Pseudemys scripta. J Comp Neurol 261:319–346Google Scholar
  49. Thexton AJ, Wake DB, Wake MH (1977) Tongue function in the salamander Bolitoglossa occidentalis. Arch Oral Biol 22:361–366Google Scholar
  50. Udin SB (1987) A projection from the mesencephalic tegmentum to the nucleus isthmi in the frogs, Rana pipiens and Acris crepitons. Neuroscience 21:631–637Google Scholar
  51. Udin SB, Fisher MD (1985) The development of the nucleus isthmi in Xenopus laevis I. Cell genesis and the formation of connections with the tectum. J Comp Neurol 232:25–35Google Scholar
  52. Wang S, Yan K, Wang Y (1980) Visual field topography and binocular responses in frog's nucleus isthmi. Scientia Sinica Vol XXIV No 9:1292–1301Google Scholar
  53. Wang S, Yan K, Wang Y (1981) Visual field topography in the frog's nucleus isthmi. Neurosci Lett 23:37–41Google Scholar
  54. Wang S, Yan K, Wang Y (1982) Nucleus isthmus of toad is secondary visual center. Scientia Sinica Vol XXV No 11:1172–1178Google Scholar
  55. Wang S, Yan K, Wang Y, Jiang S, Wang X (1983) Neuroanatomy and electrophysiology of the lacertilian nucleus isthmi. Brain Res 275:355–360Google Scholar
  56. Welker E, Hoogland PV, Lohman AHM (1983) Tectal connections in Python reticulatus. J Comp Neurol 220:347–354Google Scholar
  57. Wiggers W (1991) Elektrophysiologische, neuroanatomische und verhaltensphysiologische Untersuchungen zur visuellen Verhaltenssteuerung bei lungenlosen Salamandern. Diss Universität BremenGoogle Scholar
  58. Wilczynski W, Northcutt RG (1977) Afferents to the optic tectum of the leopard frog: An HRP study. J Comp Neurol 173:219–230Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • Wolfgang Wiggers
    • 1
  • Gerhard Roth
    • 1
  1. 1.Institut für Hirnforschung, Universität BremenBremen 33FRG

Personalised recommendations